TY - JOUR
T1 - Distinct synchronization, cortical coupling and behavioral function of two basal forebrain cholinergic neuron types
AU - Laszlovszky, Tamás
AU - Schlingloff, Dániel
AU - Hegedüs, Panna
AU - Freund, Tamás F.
AU - Gulyás, Attila
AU - Kepecs, Adam
AU - Hangya, Balázs
N1 - Funding Information:
We thank J. Szabadics, V. Varga, L. Acsády, N. Hádinger and G. Buzsáki for insightful discussions and comments on the manuscript and K. Sviatkó for help with graphics in Fig. 8. This work was supported by the ‘Lendület’ Program of the Hungarian Academy of Sciences (LP2015-2/2015), NKFIH KH125294 and the European Research Council Starting (grant no. 715043) to B.H., NKFIH K115441 and KH124345 to A.G., NINDS R01NS088661, R01NS075531 and McKnight Cognitive Disorders Award to A.K., ÚNKP-19-3 New National Excellence Program of the Ministry for Innovation and Technology to P.H., and EFOP-3.6.3-VEKOP-16-2017-00009 to D.S. and T.L. B.H. is a member of the FENS-Kavli Network of Excellence.
Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.
PY - 2020/8/1
Y1 - 2020/8/1
N2 - Basal forebrain cholinergic neurons (BFCNs) modulate synaptic plasticity, cortical processing, brain states and oscillations. However, whether distinct types of BFCNs support different functions remains unclear. Therefore, we recorded BFCNs in vivo, to examine their behavioral functions, and in vitro, to study their intrinsic properties. We identified two distinct types of BFCNs that differ in their firing modes, synchronization properties and behavioral correlates. Bursting cholinergic neurons (Burst-BFCNs) fired synchronously, phase-locked to cortical theta activity and fired precisely timed bursts after reward and punishment. Regular-firing cholinergic neurons (Reg-BFCNs) were found predominantly in the posterior basal forebrain, displayed strong theta rhythmicity and responded with precise single spikes after behavioral outcomes. In an auditory detection task, synchronization of Burst-BFCNs to the auditory cortex predicted the timing of behavioral responses, whereas tone-evoked cortical coupling of Reg-BFCNs predicted correct detections. We propose that differential recruitment of two basal forebrain cholinergic neuron types generates behavior-specific cortical activation.
AB - Basal forebrain cholinergic neurons (BFCNs) modulate synaptic plasticity, cortical processing, brain states and oscillations. However, whether distinct types of BFCNs support different functions remains unclear. Therefore, we recorded BFCNs in vivo, to examine their behavioral functions, and in vitro, to study their intrinsic properties. We identified two distinct types of BFCNs that differ in their firing modes, synchronization properties and behavioral correlates. Bursting cholinergic neurons (Burst-BFCNs) fired synchronously, phase-locked to cortical theta activity and fired precisely timed bursts after reward and punishment. Regular-firing cholinergic neurons (Reg-BFCNs) were found predominantly in the posterior basal forebrain, displayed strong theta rhythmicity and responded with precise single spikes after behavioral outcomes. In an auditory detection task, synchronization of Burst-BFCNs to the auditory cortex predicted the timing of behavioral responses, whereas tone-evoked cortical coupling of Reg-BFCNs predicted correct detections. We propose that differential recruitment of two basal forebrain cholinergic neuron types generates behavior-specific cortical activation.
UR - http://www.scopus.com/inward/record.url?scp=85086721858&partnerID=8YFLogxK
U2 - 10.1038/s41593-020-0648-0
DO - 10.1038/s41593-020-0648-0
M3 - Article
C2 - 32572235
AN - SCOPUS:85086721858
SN - 1097-6256
VL - 23
SP - 992
EP - 1003
JO - Nature neuroscience
JF - Nature neuroscience
IS - 8
ER -